The expressive pattern of laughter

Abstract

Laughter as a vocal expressive-communicative signal is one of the least understood and most frequently overlooked human behaviors. The chapter provides an overview of what we know about laughter in terms of respiration, vocalization, facial action, and body movement and attempts to illustrate the mechanisms of laughter and to de - fine its elements. The importance of discriminatin g between spontaneous and con- trived laughter is pointed out and it is argued that unrestrained spontaneous laughter involves inarticulate vocalization. It is argued that we need research integrating the different systems in laughter including experience. Laughter is a conspicuous but frequently overlooked human phenomenon. In ontogenetic development it emerges, later than smiling, around the fourth month; however, cases of gelastic epilepsy (from Greek; gelos = laughter) among neonates demonstrate that all structures are there and functional on date of birth. Further evidence for its innateness comes from twin studies as well as from the fact that laughter is easily observable among deaf-blind children (even among deaf-blind thalidomide children, who could not "learn" laughter by touching people's faces). Man is not the only animal that laughs. Like smiling, laughter has its equivalent in the repertoire of some nonhuman primates. Beginning with Darwin (1872), many writers have been struck by the notable acoustic, orofacial, and contextual similari- ties between chimpanzee and human laughter. Especially among juvenile chim- panzees a "play-face" with associated vocalization was noted to accompany ac- tions such as play, tickling, or play-biting (Preuschoft, 1995; van Hooff, 1972). 1. Laughter as an Inarticulate Utterance

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THE EXPRESSIVE PATTERN OF LAUGHTER
WILLIBALD RUCH* and PAUL EKMAN°
*Department of Physiological Psychology, Heinrich-Heine-Universität Düsseldorf,
Universitätsstraße 1, 40225 Düsseldorf, Germany
°Human Interaction Laboratory, University of California as San Francisco, 401
Parnassus Avenue, San Francisco 94143, USA
ABSTRACT
Laughter as a vocal expressive-communicative signal is one of the least understood
and most frequently overlooked human behaviors. The chapter provides an overview
of what we know about laughter in terms of respiration, vocalization, facial action,
and body movement and attempts to illustrate the mechanisms of laughter and to de-
fine its elements. The importance of discriminating between spontaneous and con-
trived laughter is pointed out and it is argued that unrestrained spontaneous laughter
involves inarticulate vocalization. It is argued that we need research integrating the
different systems in laughter including experience.
Laughter is a conspicuous but frequently overlooked human phenomenon. In
ontogenetic development it emerges, later than smiling, around the fourth month;
however, cases of gelastic epilepsy (from Greek; gelos = laughter) among neonates
demonstrate that all structures are there and functional on date of birth. Further
evidence for its innateness comes from twin studies as well as from the fact that
laughter is easily observable among deaf-blind children (even among deaf-blind
thalidomide children, who could not "learn" laughter by touching people's faces).
Man is not the only animal that laughs. Like smiling, laughter has its equivalent
in the repertoire of some nonhuman primates. Beginning with Darwin (1872), many
writers have been struck by the notable acoustic, orofacial, and contextual similari-
ties between chimpanzee and human laughter. Especially among juvenile chim-
panzees a "play-face" with associated vocalization was noted to accompany ac-
tions such as play, tickling, or play-biting (Preuschoft, 1995; van Hooff, 1972).
1. Laughter as an Inarticulate Utterance
Laughter is estimated to be about 7 million years old (Niemitz, 1990). There is
disagreement on how human speech developed phylogenetically. It could have
originated from non-verbal vocal utterances, a prelingual gestural system, or sounds
initially used to supplement the facial channel. However, it is safe to assume that
laughter –like other utterances such as moan, sigh, cry, groan, etc.– was there before
man developed speech and served as an expressive-communicative social signal.
Considering the stage in the evolution of voice when laughter emerged allows us
to make several deductions about the nature of the sound, its generation and the

cerebral organization of laughter. If laughter was part of the human vocal repertoire
before the speech centers were developed, it is likely that the sound was generated
almost exclusively by laryngeal modulations, modified to some degree by suprala-
ryngeal activity but not by articulation. This is because articulation requires volun-
tary control over the vocal system. Thus the production of speech sounds needs
the coordination of respiration, phonation, resonance, and articulation, an analysis
of laughter will involve mainly the consideration of the first three. But is it consis-
tent with current knowledge to hypothesize that a laugh-pulse –a vocalization seg-
ment initiated by an aspirated "h" type sound followed by the utterance of one of
several vowel sounds that is then abruptly terminated– is an inarticulate sound? In-
deed, the /h/, an voiceless fricative glottal sound, is the only consonant produced at
the level of the larynx; but as laughter is not "speech" we should not expect
phonemes of a language to be uttered. Likewise, the assumption of resting articula-
tors would suggest that the laughter "vowel" (but also the sound for other prelin-
gual utterances, such as moaning or utterances of astonishment) is the central vowel
schwa, or /e/ (as in about). For the production of this "neutral vowel" one needs to
open the mouth and lower the jaw, but keep all other articulators passive. We know
from everyday experience that there is a tremendous variety in the quality of the
laughing sounds, so obviously deviations from the schwa occur. This does not con-
tradict the hypothesis of an inarticulate vocalization per se but puts forward the
task of defining the deviations from the resting articulation position that are due to
altered emotional states and separate them from those supralaryngeal conditions
modulating the sound that are due to voluntary actions.
A second factor that we need to take into account is that there are different
ways to generate laughing sounds and it is possible to intentionally modulate the
emotion-driven spontaneous laughter. As the cerebral organization of vocal behav-
ior progressed phylogenetically after these early facio-vocal signals became hard-
wired, higher centers obtained control over the laughter "timer". Thus, in addition to
laughing spontaneously (emotional laughter), we can laugh voluntarily or on com-
mand (contrived or faked laughter), and we can even speak or sing the laughing
sounds, which typically are phonetically represented as "ha ha ha." These forms of
utterances differ in degree of volitional control and –inversely– emotionality, and
imply different neural pathways and systems involved (for reviews of neuronal
control of vocalization see, for example, Jürgens, 1998; Ploog, 1986; for reviews or
models of laughter: Arroyo et al., 1993; Fried et al., 1998). The distinction made be-
tween spontaneous and voluntary laughter is consistent with clinical observations;
certain patients with degenerative brain disorders may be unable to move their ab-
domen voluntarily, but demonstrate vigorous expiratory movement of the abdomen
when laughing spontaneously (Bright et al., 1986). Finally, it should be noted that
there are also voluntary attempts to regulate spontaneous laughter; for sake of
brevity the combination of voluntary and spontaneous in regulated laughter is only
mentioned here.

In spontaneous laughter we are following an impulse, an urge to laugh without
restraining ourselves. There is no attempt to suppress the response or exert any
control over its expression; the laughing person has been described as abandoning
himself or herself to the body response (Plessner, 1941). The involuntary aspect
can also be seen in the fact that during laughter our self-awareness and self-attention
is diminished. Trying to direct attention during a laughter episode stops or reduces
laughter. During laughter the state of consciousness is altered; as Hall and Allin
(1897; p. 8-9) put it: "[t]he objective world has vanished and is forgotten, the pro-
prieties and even the presence of others are lost, and the soul is all eye and ear to
the one laughable object. Care, trouble, and even physical pain are forgotten, and
the mind, as it were, falls back through unnumbered millennia and catches a glimpse
of that primeval paradise where joy was intense and supreme." While descriptions
of emotional experience are rather sparse and reports of subjects mainly refer to the
awareness of the impulse to laugh, spontaneous laughter is clearly enjoyable.
In voluntary laughter we may want to produce a sound pattern like that of nat-
ural laughter. A typical everyday situation demanding faked laughter is when we
want to signal somebody that we enjoyed a humorous message and join the laughter
of others but actually do not feel any enjoyment. While voluntary laughter may
pass over into involuntary laughter, we can not voluntarily produce emotional
laughter. Interestingly, research has shown that contrived and spontaneous laughter
within a person are strikingly similar with respect to the respirational pattern
(suggesting a "laughter signature"); however, it is doubtful whether this is also the
case for supralaryngeal systems. The many ways in which they differ still need to
be described; this will be especially important when studying individual differences
as laughter gets socialized during ontogenetic development. Research has made use
of the fact that we can voluntarily alter key features, and thus studies of laughter at
different vowels, pitch, and voice quality exist (Citardi et al., 1996; Habermann,
1955). Laughing on command is embarrassing to some, and thus the results obtained
for contrived laughter are of limited value for describing spontaneous laughter as it
may merge voluntary movements with unintended affective states.
Speaking or singing "ha ha" allows modulating the sound in many ways (e.g.,
stretching the length of vowels, emphasizing particular syllables), just as with other
spoken words. As with voluntary laughter we intend to produce a particular sound
pattern and we have even more control over the outcome; the major difference being
that phonation is not based on forced breathing but on well dosed air supply result-
ing in less tracheal resonance, breathiness, and aspiration. Spoken laugh sounds may
be devoid of emotional intonation; thus there will be less variability in melody, and
the utterance will be more clearly articulated and often match the phonemes of a
language. Emotional laughter and speech are rather independent; in fact, laughter and
speech may co-occur, thereby lengthening the duration of laugh-pulses (Nwokah et
al., in press). It remains to be verified that damage of the higher speech centers has
little impact on the expression of tickle-induced emotional laughter.

2. Description of Laughter
Laughter is not a term used consistently, nor is it precisely defined in research
articles and even encyclopedias. In everyday life a smiling face is often referred to
as "laughter" although the vocal element is entirely missing. Research studies usu-
ally focus on one or two systems of laughter rather than the integration of all the
components involved. For example, a study of the acoustics of laughter typically
restricts the investigation to the phonatory system and may arrive at the conclusion
that the duration of laughter is, say, below two seconds. Sound production is con-
tingent on air flow and the deviation from resting breathing exceeds the rhythmic
forced exhalations underlying laughter by far; therefore duration estimates of eight
seconds are not uncommon in respiration studies (e.g., Habermann, 1955). In stud-
ies of primate laughter the face gets most attention and also studies of joy in hu-
mans typically focus on the face, or even on the emotion-specific actions neglecting
the mouth opening altogether. The analysis of videotaped laughter suggests a mean
duration of five seconds while the study of facial muscle contractions exceeds this
value due to the offset period where facial changes are barely visible (Ruch, 1990).
2.1. Laughter Segmentation
Laughter bout. The term laughter bout is used here to refer to the whole behav-
ioral-acoustic event, including the respiratory, vocal, and facial and skeletomuscular
elements. Prototypically, a laughter bout may be subdivided into an onset (i.e., the
pre-vocal facial part which in explosive laughter is very short and steep); an apex
(i.e., the period where vocalization or forced exhalation occurs), which –in sustained
laughter– might be interrupted by inhalations; and an offset (i.e., a post-vocalization
part; usually a long-lasting smile fading out smoothly).
Laugh cycle and laugh-pulse. The laughter vocalization period is composed of
laugh cycles, i.e., repetitive laugh-pulses (Moore & von Leden, 1958) interspersed
with pauses. There is laughter with only one or two pulses ("exclamation" laughter,
"chuckle"; Nwokah et al., 1993), but studies typically report a mode of four pulses
in a laugh cycle (Provine & Yong, 1991; Rothgänger et al., 1998). The upper num-
ber of pulses in a laugh cycle is limited by the lung volume, and different studies
give numbers between 9 and 12 (Boeke, 1899; Provine & Yong, 1991); a laughter
episode –two or more laughter bouts separated by inspirations– will have more.
Table 1 presents an attempt to integrate empirical findings from studies of dif-
ferent systems involved in laughter. Obviously the same phenomenon was studied
and converging information about the rhythmic pattern of laugh-pulses can be ex-
tracted from studies of air flow and pressure, respirational and laryngeal muscles,
acoustics, and the oscillations in the pressure a finger puts on a plate. During in-
tense laughter, the laugh-pulse would be extractable from different parts of the
body, as the massive respiration movements cause vibrations of the trunk and limbs
to occur which may be detected by an acceleration sensor on the body surface.

Table 1. The laugh-pulse as studied in respiration, acoustics, and body movement
Author(s) variable studied number of duration (in ms)
pulses IPI pulse IPP
Respiration
Bloch, Lemeignan and Aguilera (1991) rectus abdominis muscle (EMG) 4.17/s 240
Hoit, Plassman, Lansing and Hixon (1988) rectus abdominis muscle (EMG) 5-6/s
Air pressure
Agostoni, Sant'Ambrogio and Portillo Carrasco (1960) gastric air pressure (swallowed balloon) 5-6 cycles/s
thoracic air pressure (swallowed balloon) 5-6 cycles/s
Schroetter (1925) exhaled air in closed system up to 5/s
Laryngeal activity
Moore and van Leden (1958) vocal fold vibrations (ultra high speed camera) 30-100
Luschei, Ramig, Baker and Smith (1997) thyroarytenoid muscle (EMG) 5 Hz
cricothyroid muscle (EMG) 5 Hz
posterior cricoarytenoid muscle (EMG) 5 Hz
Acoustics
Boeke (1899) "ha"-sounds/utterances 4.12/s 243 60 183
Bickley and Hunnicutt (1992) laughter syllables 204 97 167
laughter syllables 224 68 156
Nwokah, Davies, Islam, Hsu and Fogel (1993) laugh events 200
Nwokah, Hsu, Davies and Fogel (1998) events 110
events 130
Mowrer, LaPointe and Case (1987) laugh bursts 5.55/s 180
Provine and Yong (1991) laughter notes 4.76/s 210 75 135
Rothgänger, Hauser, Cappellini and Guidotti (1998) plosives 4.67/s 213 126 87
Body vibrations (sentics)
Clynes (1980) transient finger pressure (sentograph) 5.03/s 199
Notes. Authors typically gave either frequency per second or the duration of utterances, or other information which was then transformed into one
or both parameters by the author of the present chapter.
IPI = interpulse interval; IPP = interpulse pause

While so far there is no convincing evidence for Darwin's (1872) claim that the
muscles of the limbs are thrown into rapid vibratory movements at the same time
as the respiratory muscles, initial support can be found in a sample figure provided
by Santibañez and Bloch (1986). In this illustration of the EMG-recordings from
the brachioradialis (forearm muscle which bends the elbow) and rectus femoris
(anterior muscle of the upper thigh) muscles, an increase in amplitude can be found,
and the rhythmic pattern seems to match the one of the abdominal muscles.
There are roughly five pulses per second, but the interpulse interval varies as a
function of the position of the pulse in a sequence (Boeke, 1899; Provine & Yong,
1991; Rothgänger et al., 1998). Further segmentation of the laugh-pulse can be ob-
tained in the different systems involved in laughter. Boeke, recording his own laugh-
ter on an Edison Sonograph, already discovered the existence of pauses between the
laughter sound pulses whose length exceeded the duration of the ha-utterances by a
factor of two. Due to the dynamics of respiration, the duration of sound pulses de-
creases sequentially from an earlier to later position, and the duration of the inter-
pulse pause increases. Differences in operational definitions of pulse and interpulse
pause add further variations to the estimations of length (see Table 1).
Acoustic segmentation of the laugh-pulse. Acoustic analyses of laughter suggest
a distinction between the vowel-like utterance nucleus and the preceding aspirated
"h"-type sound initiating the sound pulse. As the glottis is open during the inter-
pulse pauses, aspiration continues. Thus, not surprisingly, Provine and Yong
(1991) report that laughter played backwards still sounds like "ha ha".
Vibratory movements in a laugh-pulse. At the level of laryngeal movements a
laugh-pulse can be further split up into the number and duration of vibratory cycles
of the vocal cords, and even further into their contour; i.e., the phases of when vo-
cal cords are opening, closing, or closed. Using ultra high speed motion picture pho-
tography (4000 exposures a second), Moore and van Leden (1958) found in their
analysis of the vibration of the cords during a man's laughter a range of 5 to 15 cy-
cles of opening and closing in laugh-pulses. Accordingly, the duration of laugh-
pulses varied from 30 to 100 ms. Each vibratory cycle interrupts the air column as-
cending from the lungs and the rate of these cycles is the basis for the fundamental
frequency of the sound. Further segmentation may be achieved by analyzing the
time when vocal cords are opening, closing, or closed, and this vibratory curve con-
tour reflects the dynamics of respiration as it undergoes a progressive change even
within one laugh-pulse. These modifications in the vibratory pattern codetermine
how laughter sounds and may be a key factor in distinguishing types of laughter.
2.2. Laughter Respiration
A respiration cycle consists of inspiration, inspiration pause, expiration, and
expiration pause. No matter where in a respiration cycle a person is, laughter typi-
cally begins with an initial forced exhalation, followed by a more or less sustained
sequence of repeated expirations of high frequency and low amplitude, which may

or may not be phonated as "ha ha ha;" i.e., the laugh cycles. While in the case of
sustained laughter the expiratory phases will be interrupted by inhalations, there is
no evidence for Darwin's (1872; p. 199) assertion that "... [t]he sound of laughter is
produced by a deep inspiration followed by short, interrupted, spasmodic contrac-
tion of the chest, and especially of the diaphragm." No inspiration preceding the
laugh is necessary as laughter is produced at a low lung volume (Bright et al., 1986).
Normally the laugh cycles are initiated around functional residual capacity (FRC;
i.e., at the lung volume after a normal expiration) and terminate close to residual
volume (i.e., the air volume remaining in the lung after maximal expiration), or
sometimes even exceed the level of maximal voluntary exhalation (Bright et al.,
1986; Lloyd, 1938). Thus, most likely the initial forced exhalation is expelling the
tidal volume, and the following sequence of laugh-pulses is based on the expiratory
reserve volume. The increase in depth of respiration –the amplitude during laughter
may be up to 2.5 times higher than during resting respiration– is therefore due to
the stronger expiration; inspiration may add to the amplitude in case of laugher
episodes, where single deep inhalations intersperse the expiratory sequences.
The rhythmic laughter respiration pattern is produced by saccadic contractions
of auxiliary expiration muscles; i.e., muscles that are typically passive during nor-
mal expiration, such as the diaphragm (Agostoni et al., 1960), the abdominal (rectus
abdominis; Hoit et al., 1988; Santibañez & Bloch, 1986) and the rib cage muscles
(triangularis sterni; De Troyer et al., 1987). Of the three muscles mentioned, only
the diaphragm is involved in resting breathing in humans; its contraction causes in-
spiration. The role of the diaphragm is not entirely clear, however, as the discharges
in the EMG recordings (albeit parallel to the air pressure) may be indicating reflex
contractions due to the passive distention occurring as a function of the violent con-
tractions of the ribcage and abdominal muscles. The triangularis sterni is passive
during quiet breathing but involved in different active respiration maneuvers; i.e.,
respiration below FRC. It contributes to the deflation of the rib cage during active
expiration such as in coughing and its neural activation is largely coupled with that
of the abdominals. The relative contribution of rib cage and abdomen to the volume
may vary even within one laughter cycle (Bright et al., 1986; Habermann, 1955).
The respiratory muscles function in concert with the larynx; while without any
closing of the glottis there may be single or a few forced exhalations, the adduction
(closing) prevents the air to be exhaled too quickly, and allows the building up and
maintaining of subglottal air pressure. The initial forced exhalation increases the
transdiaphragmatic air pressure by about 5440 Pa (Agostoni et al., 1960) to about
6120 Pa (Schroetter, 1925); this pressure plateau is maintained and forms the basis
for the sustained period of phonation of the laugh utterances. The heightened pres-
sure makes the air stream up the airways through the larynx where the rhythmic
closing and opening of the glottis interrupts the air stream. These vibrations are
carried through the vocal tract whose shape amplifies or dampens certain frequency
spectra, and finally the air escapes through the mouth or the nose.

2.3. Phonation
The acoustic sequence of laughter pulses are produced by a series of rapid, con-
tinuous, stereotypic laryngeal adjustments, which are separated into four stages: in-
terpulse pause, adduction (closing) of the arytenoid cartilages, vibration of vocal
chords, and abduction (opening) of the arytenoid cartilages (Moore & von Leden,
1958). As confirmed by laryngeal EMG during laughter the thyroarytenoid and –to
a lesser extent– the cricothyroid muscles are involved in the closing of the glottis
and the opening is achieved by the posterior cricoarytenoid muscle (Luschei et al.,
1997). Both groups contract in the same pace (see Table 1), but with a time lag.
The interpulse pause is an instant of quiet between the audible moments of
laughter. The arytenoid cartilages rest open allowing the breath stream to flow
unimpeded through the larynx, and the vocal cords remain motionless. Some of the
aspirate sound is produced at this time but becomes more audible as the vocal cords
approach each other. The fact that the "h" sound is an eddy-current phenomenon
created during the closing stage of the valve-like movements of the vocal folds is in
line with the assumption of the absence of cortically controlled articulation. Occa-
sionally it was argued that glottal stops occur between the laugh-pulses; however,
both videoendoscopy and photoglottography show that the glottis is widely open
at the end of a laugh-pulse (Citardi et al., 1996; Moore & van Leden, 1958) and the
acoustic analyses reported quiet aspirations in the periods between voicing (e.g.
Luschei et al., 1997).
During the adduction stage the arytenoid cartilages carry the cords toward each
other and when the glottal space has been narrowed to a small slit, the cords begin
to vibrate. As vibration occurs not only when the arytenoids are fully approxi-
mated but start at the end of the adduction and continue when abduction starts
again there are transitions between an initial swing of the flaccid cords and the full
vibrations and again towards the end of the vibratory movements. Moore and von
Leden (1958) report that it takes about 10 ms to accomplish the transition from
quiescence to full vibration, and that changes in vibratory curve contours and in the
length of cycles occur as the laugh-pulse progresses. During the adduction phase of
the laugh-pulse the arytenoids and vocal cords move into their rest positions. There
is a progressive diminution of the mesial excursion of the cords and the slowing of
the cord movement as the interarytenoid space enlarges; for example, in the sample
laugh-pulse provided by Moore and von Leden (1958) there is a progressive drop
of about 30 cycles per second.
Thus, whereas during singing we try to keep the fundamental frequency con-
stant for each note, due to the dynamics of air flow there is tremendous variation
even within a single laugh-pulse. Acoustic analyses also demonstrate the changes in
fundamental frequency between laugh-pulses; typically there is a progressive de-
crease in pitch and intensity (loudness) of laughter at later pulses of a cycle. Boeke
noted already in 1899 that the melodic variation in laughter is higher than in speech.

2.4. Supralyrangeal Modulation
The buzzing sound produced in the glottis is carried into the resonance tract
whose form codetermines the sound of laughter. While the laryngeal and respiratory
movements during laughter appear to be highly stereotyped, the acoustic output is
quite variable. There is little systematic research on the activity of the 10 or so
movable articulators and thus at present a comprehensive evaluation whether the
activity is compatible with the hypothesis of an inarticulate sound is not possible.
While one could predict that in courteous laughter without much emotional in-
volvement the vowel uttered is schwa-like, in emotional laughter some supralaryn-
geal conditions modulating the sound occur, partly molded by the emotional state.
Despite the assumption that there is no cortically controlled articulation in laughter,
qualitative differences might be related to emotional states in various ways. Varia-
tions in pitch can be obtained by increasing or reducing the length of the vocal tract,
for example, by lifting or lowering the larynx, or by protruding or retracting the
lips. Indeed, both Habermann (1955) and Citardi et al. (1996) observed movement
of the larynx in the superior–inferior direction during voluntary laughter. A further
determinant of pitch, the lengthening and tension of the vocal cords, is susceptible
to emotional arousal (contraction of the vocalis muscles) as is the general degree of
tension vs. relaxation in the laryngeal area. Width or narrowness of the pharynx af-
fects the voice quality, and it has been argued that in positive states there is a
widening of the throat (as in taking up food) producing a-type sounds while in dis-
gust there is a narrowing of the throat (as in expelling bad food) compatible with the
sound during contemptuous or scornful laughter.
Of the major articulators in speech, the tongue (involved in producing high and
low, and front and back vowels) is likely to be in a resting central position during
joyful laughter, but the jaw and lips are not. The act of opening the mouth and the
degree of aperture of the mouth (i.e., lowering of the jaw) affects the sound; this
action is coupled with respiration (allows the escape of air). Habermann (1955) re-
ported nasals occurring; this seems to be likely only for mild laughter, when the
mouth is not opened, the soft palate lowered, and the air escapes through the nose.
Last but not least, two important articulators, the lips and the cheeks, are typically
not in a resting position as they are part of the emotion-driven facial actions. For
example, the facial display of enjoyment involves the retraction of the lip corners
and the cheeks are lifted upwards (see description of the specific muscles in section
2.5 below); the contraction of these two pairs of muscles changes the form of the
mouth aperture and tenses the skin of the upper ending of the vocal tract thereby
affecting the sound at the onset and apex of these actions. As Tartter (1980)
demonstrated, the same spoken message sounds different when the sender is smil-
ing or showing a resting face; listeners can reliably infer smiling from the voice. In-
tense smiling is also incompatible with the utterance of vowels which require a pro-
truding of the lips, such as an "o" or "u," making these sounds unlikely to occur

during joyful laughter. Taken together, these considerations would predict that
laughter vowels would deviate from being a neutral vowel and the reason for a con-
trary finding is due to other constraints during emotional laughter.
Chimpanzee laughter. As the laryngeal apparatus and vocal tract of humans
and primates are different in many ways (see Lieberman, 1975) one should not
expect the similarities between primate and human laughter to be very strong.
Chimpanzee laughter has been described as a soft repetitive guttural sound of low
intensity panting noises during exhalation that roughly sounds like human laughter.
The sound is based on rhythmic breathing resulting in staccato vocalizations.
Spectro graphic analyses are sparse; Berntson et al. (1989) report that while
generally "noisy," the laughter recordings from a juvenile male during active play
evidenced temporal structure, with periodic louder voiced and voiceless
components. They provide a sample figure with four distinct syllable-like louder
egressive voiced segments. These segments were characterized by some low
fundamental frequency voicing, with intermittent noise. Provine (1996) concludes
that the major difference is that in human laughter several laugh-pulses may occur
on one expiration, whereas chimpanzee laughter is produced during each brief
expiration and inspiration. He notes that "... [t]he sounds of chimpanzee and human
laughter are sufficiently different that without viewing the characteristic "play face"
and source of stimulation (such as play and tickle), naive human beings may be
unable to identify the chimpanzee vocalization as laughter" (Provine, 1996; p. 40).
2.5. Facial Actions
If the theory applies that sounds were initially added to the facial display to
supplement or underscore a message then the emotion-specific facial configuration
molded and also limited the sound utterance. Thus, the identification of the facial
actions in spontaneous laughter is important. As laughter is commonly associated
with the emotion of joy, the facial configuration named (Ekman et al., 1990) the
Duchenne display (to honor Duchenne who first described how this pattern distin-
guished enjoyment smiles from other kinds of smiling) might serve as a first starting
point against which, for descriptive purposes, deviations may be judged. The
Duchenne display refers to the joint contraction of the zygomatic major and orbicu-
laris oculi muscles (pulling the lip corners backwards and upwards and raising the
cheeks causing eye wrinkles, respectively). While laughter has been described as oc-
curring during different emotional states, so far it is not clear whether or not these
laughs are also morphologically different. Furthermore, those voluntary facial ac-
tions aimed at modulating the intensity, duration or quality of the sound emitted, or
to suppressing laughter altogether are not completely identified. Another starting
point may be the facial display during primate laughter. This is circular, in part, as
the human facial actions have been the basis for homologizing the primate displays.
Primate laughter. The facial features of primates have been described by salient
features, rather than their muscular underpinning. The play face (or relaxed open-

mouth display) in chimpanzees has been described as the jaws being widely open,
the mouth corners normal or slightly retracted, the upper lip covering the teeth,
lower lips loose, and the lower teeth exposed. This description seems to involve the
action of the zygomatic major, but not the orbicularis oculi muscles, although it is
developed in chimpanzees. However, most of this work (e.g., Chevalier-Skolnikoff,
1973; van Hooff, 1972) was done before the rediscovery of Duchenne, and there-
fore the actions of this muscle were perhaps not specifically studied.
Human laughter. The facial expression of laughter has been given some atten-
tion by researchers during the past and present century. A summary of hypotheses
put forward and the results of some studies of laughter using facial-EMG (surface
and needle electrodes) or the Facial Action Coding System (Ekman & Friesen, 1978)
are presented in Table 2. It should be noted, however, that early descriptions had to
be based on real time observations, or on inferences from knowledge about facial
musculature since no recording tools were available. As intense laughter involves
movement of head and trunk, facial measurement continues to be a problem.
Table 2 confirms that the two muscles forming the Duchenne smile have been
found to be involved in laughter as well, explaining the smooth transitions between
smiling and laughter in both the onset and offset of a laughter bout. Sumitsuji (pers.
comm.) observed that there is little innervation of the orbicularis oculi muscle dur-
ing voluntary laughter; thus the eye region might serve as a marker for distinguishing
emotional from voluntary laughter, much as it does for distinguishing enjoyment
from non enjoyment smiling. Interestingly, in two forms of pathological laughter
(epileptic laughter and pseudo bulbar palsy; representing excitation or the loss of
inhibition, respectively), the activated motor pattern includes the contraction of the
orbicularis oculi muscle. Furthermore, laughter includes the relaxation of some mus-
cles (masseter, pterygoids) allowing for a lowering of the lower jaw so that the air is
expelled through the mouth.
However, the number of postulated and confirmed muscles involved in the
laughter facial expression are far more than those usually identified. So how do we
make sense of the true complexity of the neuromuscular patterns of laughter given
the limited and contradictory information currently available? First, several of the
additional muscles may be involved in auxiliary movements, perhaps of secondary
importance; this might be the case for the muscles located around the mouth, such
as the levator labii superioris, depressor anguli oris, risorius, or orbicularis oris.
They are involved in the radial opening of the lips aimed at widening the mouth to
let the air stream out more easily. Second, some of the hypotheses relate to the in-
tensity of laughter. It has been suggested that strong laughter also involves the mus-
cles in the upper face, such as the corrugator supercilii and the frontalis muscles.
Moreover, claims have been made that with increasing intensity of laughter almost
all muscles get involved and tensed (Heller, 1902) and that the most intense form of
laughter is not well distinguishable from the facial display of crying (Darwin, 1872;
Piderit, 1867). There is no support for this from the existing studies of healthy

Table 2. Hypotheses and empirical findings regarding the involvement of facial muscles in laughter
upper face muscles mid-face muscles lower face muscles
Author(s) 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18
Hypotheses: laughter
Bloch et al. (1987) X X X X
Darwin (1872) X X X X X?
Dearborn (1897) X X X X X X X X X X
Hecker (1873) X X X
Heller (1902) X X X X
Hjortsjö (1970) X X X X X X X X X X
Piderit (1867) X X X X X
Poeck and Pilleri (1963) X X X X
Raulin (1900) X? X X X
Hypotheses: strong laughter
Darwin (1872) X X X X X X?
Heller (1902) X X X X X X X X X X
Piderit (1867) X X X X X X
Results: FACS-studies
Grammer (1990) X
Keltner and Bonanno
(1997)
X X –
Ruch (1990, 1994) X X X –
Ruch (1997) X X –
Results: EMG-studies
Gallo and Palla (1995) X
Santibañez et al. (1986) X X
Sumitsuji (1967) – – – X X X X X X X
Tanaka (1976) – – – X X X
Tanaka et al. (1991) – – – X X X X X
Supressed laughter
Tanaka (1976) X X X X
Pathological laughter
Tanaka et al. (1991) X X X X X X X X
Yamada et al. (1994) X
Notes. 1=frontalis, pars medialis-raises the inner brows, producing horizontal furrows in the medial
region of the forehead; 2=frontalis, pars lateralis-raises the outer brows, producing horizontal
furrows in the lateral regions of the forehead; 3=corrugator supercilii-draws the brows together and
downward, producing vertical furrows between the brows; 4=pyramidalis/procerus/depressor
supercilii-pulls the medial part of the brows downward and may wrinkle the skin over the bridge of
the nose; 5=orbicularis oculi, pars orbitalis-tightens the skin surrounding the eye causing crows-feet
wrinkles; 6=orbicularis oculi, pars palpebralis-tightens the skin surrounding the eye causing the
lower eyelid to raise; 7=zygomaticus major-pulls the lip comers up and back; 8=zygomaticus
minor-deepens nasolabial furrow; 9=levator labii superioris/levator labii superioris, caput
infraorbitalis-raises the upper lip and flares the nostrils, exposing the canine teeth; 10=levator labii
superioris alaeque nasi-raises the center of the upper lip and flares the nostrils; 11=nasalis, pars
alaris bzw. dilatores nasi-dilates nostrils; 12=buccinator-compresses and tightens the cheek, forming
a dimple; 13=risorius-stretches lip corners straight to the side; 14=orbicularis oris-tightens,
compresses, protrudes, or inverts the lips; 15=depressor anguli oris-pulls the lip comers downward;
16=mentalis-raises the chin and protrudes the lower lip; 17=masseter-adducts the lower jaw;
18=caninus/levator anguli oris-pulls the lip corner up sharply and puffs up cheeks.
A "X" includes action of that muscle, a "–" means lowering of muscle tone. Authors either gave
names or picture of muscles or a description of facial appearance from which the muscle action was
then inferred utilizing the information provided by the Facial Action Coding System (Ekman &
Friesen, 1978). An "?" was added when the muscle is not entirely clear from the description given.

adults; on the contrary, Tanaka and Sumitsuji (1991) report a lowering of muscle
tone in the upper face during laughter (as has been found for the corrugator super-
cilii in smiling). However, in pathological laughter –usually of high intensity– the
frontalis and corrugator muscles are active (Tanaka & Sumitsuji, 1991). This would
seem to support an intensity hypothesis; however, as patients do not enjoy laugh-
ter fits, the additional movements might be of voluntary nature reflecting efforts to
control or suppress laughter rather than being part of an innate response pattern.
Third, some muscles may be active only part of the time and the course of con-
traction of muscles over time can be different for different muscles. For example,
the masseter (chewing muscle) whose relaxation initially helps to lower the jaw,
was found to have elevated activity during laughter (Gallo & Palla, 1995; Santi-
bañez & Bloch, 1986). Unfortunately, studies often report only intensity of a
muscle contraction without considering its distribution over time. Fourth, one has
to take into account that researchers might have erred in transforming their obser-
vations into the list of muscles due to the lack of profound knowledge of the effects
of muscle contraction on the appearance on the surface at that time. This might
have resulted in identifying the wrong muscle (e.g., the early anatomists' labeling of
the "risorius" seems to imply that they considered it to be the major laughing mus-
cle), or too many muscles (e.g., the strong action of the zygomatic major is able to
cause changes –like opening the nostrils or raising the upper lips– that can also be
attributed to separate muscles). Fifth, in previous studies, the type of laughter of-
ten was not controlled for and this might account for some of the additional muscle
actions observed. Instead of pure enjoyment there might have been voluntary laugh-
ter, a blend of enjoyment with other emotions (e.g., surprise should add the eleva-
tion of the eyebrows caused by the frontalis muscles), movements associated with
regulating the intensity of laughter, attempts to suppress laughter, or even acciden-
tal movements. Of course, a significant yet unexplored remaining cause for these
surplus facial actions might be that laughter during different emotional states (e.g.,
scorn, nervousness, embarrassment) is morphologically different.
The information in Table 2 is not yet complete, as not all facial muscles have
been studied so far. It seems advisable to supplement future facial EMG-studies by
videotapes of face and body to control for the nature of movement. Furthermore, it
seems essential to vary and control for the quality of laughter, guarantee for differ-
ent intensity levels, and also examine the course of muscle contractions over time
rather than studying sheer intensity at apex. We also need to start separating volun-
tary and spontaneous actions based on the existing experience (Ekman, 1997).
Further facial changes. Several authors described a brightening of the eyes
(even among chimpanzees); the sparkling quality was explained either by enhanced
lacrimation or an enhanced tenseness owing to the contraction of the muscles
around the eye (Darwin, 1872), or that the eyeballs get filled with blood or other
fluids (due to the enhanced circulation; Piderit, 1867). Furthermore, there is the ob-
servation that a laughter episode is frequently terminated by a closing of the lids.

2.6. Body Movement
While smiling is purely facial, at higher intensity levels laughter involves the
whole body; however, changes in posture and body movements have received least
attention in the study of laughter. Darwin writes (1872; p. 206-207) "During exces-
sive laughter the whole body is often thrown backward and shakes, or is almost
convulsed." Indeed, one can expect actions associated with the respiratory move-
ments; for example, the backward tilt of the head facilitates the forced exhalations,
and the forced inhalation interrupting two laughter cycles will raise and straighten
the trunk. Furthermore, as noted above, the massive respiratory movements under-
lying the laughter pulse may cause the observed shaking of the shoulders and vibra-
tions detectable on the trunk but also extremities.
There are also actions not coupled with respiration but their exact list and the
conditions of their emergence are not known. As laboratory studies rarely induce
violent laughter one has to rely on observations and self-reports such as the one by
Hall and Allin who issued an 11 item questionnaire on tickling, fun, wit, humor, and
laughing as a supplement to The American Journal of Psychology. In a subsequent
report, they present a qualitative analyses based on responses of 3000 people (Hall
& Allin, 1897). Regarding body movements they summarize (p. 5) "... [i]n the
height of the laugh ... some plant the elbows on the knees; others rock violently
sideways, or more often back and forth; the hands are thrown into the air or
clapped on the thighs; ... the limbs jerk; the foot is stamped; the fists pound; ...
waves of nervous tremor pass over the body; ... the hand is placed over the eyes,
mouth, or both; ... little children jump up and down, lie on the floor and roll all over
the room; some swing the hands in the air; the breast heaves up and down; some
turn around on the heel from left to right ... the head shakes from side to aide; ...
others always hold the sides with both bands; others roll the head; features often
twitch or tremble convulsively." Obviously, research is needed sorting accidental
actions, attempts to regulate laughter and genuine elements of a laughter pattern.
Concluding remarks
The present review makes clear that the we need multi-level studies of laughter,
as different systems work together in the generation of the expressive pattern and
there are multiple dependencies among respiration, facial action, acoustics, and
body movements. The review was restricted to some basic elements (leaving out is-
sues such as neurohormonal effects of laughter, or social factors in laughter), since
these provide the basis for tackling the yet unanswered questions of how to detect
whether laughter is faked or felt, how to distinguish among different types of emo-
tional laughter on a morphological basis, and what is the relationship between
smiling and laughter. The list of unanswered questions and unsolved problems
seems endless, but the study of laughter is a worthwhile subject as it is a window
to ancient affective experience; a prototype of the prelingual utterance of joy.

Acknowledgments
The preparation of this chapter was facilitated by a Heisenberg grant (Ru 480/1-2)
from the German Research Council (DFG) awarded to the first author. Thanks to
Eva Nwokah and Rod Martin for comments on an earlier version of the chapter.
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